The growth speed of microtubules with XMAP215-coated beads coupled to their ends is increased by tensile force

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 36, 2013, Pages 14670-14675

  Trushko, Anastasiya ^a   Schäffer, Erik ^b,c   Howard, Jonathon ^a,d  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d YALE UNIVERSITY   (United States)

Author keywords

Microtubule dynamics; Microtubule polymerase; Optical trap

Indexed keywords

COAT PROTEIN; DIS1 PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; TOG PROTEIN; UNCLASSIFIED DRUG; XENOPUS PROTEIN; XMAP215 PROTEIN; MICROSPHERE; PROTEIN BINDING; TUBULIN; XMAP215 PROTEIN, XENOPUS;

ARTICLE; CONTROLLED STUDY; DYNAMICS; GROWTH; MICROTUBULE; MICROTUBULE ASSEMBLY; NONHUMAN; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; TENSILE STRENGTH; VELOCITY; ANIMAL; CHEMISTRY; KINETICS; METABOLISM; PHYSIOLOGY; POLYMERIZATION; SWINE; XENOPUS LAEVIS;

ANIMALS; KINETICS; MICROSPHERES; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; POLYMERIZATION; PROTEIN BINDING; SWINE; TENSILE STRENGTH; TUBULIN; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84883317619     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1218053110     Document Type: Article

References (52)

1. Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312(5991):237-242.
2. Cassimeris L, Pryer NK, Salmon ED (1988) Real-time observations of microtubule dynamic instability in living cells. J Cell Biol 107(6 Pt 1):2223-2231. (Pubitemid 19015101)
3. Sammak PJ, Borisy GG (1988) Direct observation of microtubule dynamics in living cells. Nature 332(6166):724-726.
4. Belmont LD, Hyman AA, Sawin KE, Mitchison TJ (1990) Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62(3):579-589.
5. Gard DL, Kirschner MW (1987) A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105(5):2203-2215. (Pubitemid 18019070)
6. Wang PJ, Huffaker TC (1997) Stu2p: A microtubule-binding protein that is an essential component of the yeast spindle pole body. J Cell Biol 139(5):1271-1280. (Pubitemid 27523213)
7. Cullen CF, Deák P, Glover DM, Ohkura H (1999) Mini spindles: A gene encoding a conserved microtubule-associated protein required for the integrity of the mitotic spindle in Drosophila. J Cell Biol 146(5):1005-1018. (Pubitemid 29430443)
8. Tournebize R, et al. (2000) Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat Cell Biol 2(1):13-19.
9. Garcia MA, Vardy L, Koonrugsa N, Toda T (2001) Fission yeast ch-TOG/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint. EMBO J 20(13):3389-3401. (Pubitemid 32634347)
10. Brittle AL, Ohkura H (2005) Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J 24(7):1387-1396. (Pubitemid 40593059)
11. Kawamura E, Wasteneys GO (2008) MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. J Cell Sci 121(Pt 24):4114-4123.
12. Gergely F, Draviam VM, Raff JW (2003) The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17(3):336-341. (Pubitemid 36182191)
13. Cassimeris L, Morabito J (2004) TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization, and bipolar spindle assembly. Mol Biol Cell 15(4):1580-1590. (Pubitemid 38401809)
14. Kerssemakers JWJ, et al. (2006) Assembly dynamics of microtubules at molecular resolution. Nature 442(7103):709-712. (Pubitemid 44215328)
15. Brouhard GJ, et al. (2008) XMAP215 is a processive microtubule polymerase. Cell 132(1):79-88.
16. Widlund PO, et al. (2011) XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc Natl Acad Sci USA 108(7):2741-2746.
17. Lee MJ, Gergely F, Jeffers K, Peak-Chew SY, Raff JW (2001) Msps/XMAP215 interacts with the centrosomal protein D-TACC to regulate microtubule behaviour. Nat Cell Biol 3(7):643-649. (Pubitemid 32624420)
18. Bellanger JM, Gönczy P (2003) TAC-1 and ZYG-9 form a complex that promotes microtubule assembly in C. elegans embryos. Curr Biol 13(17):1488-1498.
19. Kinoshita K, et al. (2005) Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J Cell Biol 170(7):1047-1055. (Pubitemid 41362637)
20. Tanaka K, et al. (2005) Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434(7036):987-994. (Pubitemid 40586041)
21. Kitamura E, et al. (2010) Kinetochores generate microtubules with distal plus ends: Their roles and limited lifetime in mitosis. Dev Cell 18(2):248-259.
22. Inoué S, Salmon ED (1995) Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol Biol Cell 6(12):1619-1640.
23. Yeh E, et al. (2000) Dynamic positioning of mitotic spindles in yeast: Role of microtubule motors and cortical determinants. Mol Biol Cell 11(11):3949-3961.
24. Doe CQ, Bowerman B (2001) Asymmetric cell division: Fly neuroblast meets worm zygote. Curr Opin Cell Biol 13(1):68-75. (Pubitemid 32119295)
25. Tran PT, Marsh L, Doye V, Inoué S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153(2):397- 411.
26. Gönczy P (2002) Mechanisms of spindle positioning: Focus on flies and worms. Trends Cell Biol 12(7):332-339.
27. Kusch J, Meyer A, Snyder MP, Barral Y (2002) Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev 16(13):1627-1639. (Pubitemid 34743324)
28. Howard J, Hyman AA (2003) Dynamics and mechanics of the microtubule plus end. Nature 422(6933):753-758. (Pubitemid 36514118)
29. Liakopoulos D, Kusch J, Grava S, Vogel J, Barral Y (2003) Asymmetric loading of Kar9 onto spindle poles and microtubules ensures proper spindle alignment. Cell 112(4):561-574. (Pubitemid 36263087)
30. Maekawa H, Usui T, Knop M, Schiebel E (2003) Yeast Cdk1 translocates to the plus end of cytoplasmic microtubules to regulate bud cortex interactions. EMBO J 22(3):438-449. (Pubitemid 36193589)
31. Tolic-Norrelykke S, Schäffer E, Howard J (2006) Calibration of optical tweezers with positional detection in the back focal plane. Rev Sci Instrum 77:103101.
32. Schäffer E, Nørrelykke SF, Howard J (2007) Surface forces and drag coefficients of microspheres near a plane surface measured with optical tweezers. Langmuir 23(7):3654-3665. (Pubitemid 46581890)
33. Bormuth V, Howard J, Schäffer E (2007) LED illumination for video-enhanced DIC imaging of single microtubules. J Microsc 226(Pt 1):1 -5.
34. Bormuth V, Varga V, Howard J, Schäffer E (2009) Protein friction limits diffusive and directed movements of kinesin motors on microtubules. Science 325(5942):870-873.
35. Gittes F, Schmidt CF (1998) Interference model for back-focal-plane displacement detection in optical tweezers. Opt Lett 23(1):7-9. (Pubitemid 128563619)
36. Pralle A, Prummer M, Florin EL, Stelzer EH, Hörber JK (1999) Three-dimensional high-resolution particle tracking for optical tweezers by forward scattered light. Microsc Res Tech 44(5):378-386. (Pubitemid 29122775)
37. Walker RA, et al. (1988) Dynamic instability of individual microtubules analyzed by video light microscopy: Rate constants and transition frequencies. J Cell Biol 107(4):1437-1448.
38. Fygenson DK, Braun E, Libchaber A (1994) Phase diagram of microtubules. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 50(2):1579-1588.
39. Asbury CL, Gestaut DR, Powers AF, Franck AD, Davis TN (2006) The Dam1 kinetochore complex harnesses microtubule dynamics to produce force and movement. Proc Natl Acad Sci USA 103(26):9873-9878. (Pubitemid 43993590)
40. Powers AF, et al. (2009) The Ndc80 kinetochore complex forms load-bearing attachments to dynamic microtubule tips via biased diffusion. Cell 136(5):865-875.
41. Akiyoshi B, et al. (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468(7323):576-579.
42. Oguchi Y, Uchimura S, Ohki T, Mikhailenko SV, Ishiwata S (2011) The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends. Nat Cell Biol 13(7):846-852.
43. Laan L, et al. (2012) Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 148(3):502-514.
44. Ayaz P, Ye X, Huddleston P, Brautigam CA, Rice LM (2012) A TOG:αβ-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science 337(6096):857-860.
45. Janson ME, de Dood ME, Dogterom M (2003) Dynamic instability of microtubules is regulated by force. J Cell Biol 161(6):1029-1034. (Pubitemid 36870165)
46. Wang HW, Nogales E (2005) Nucleotide-dependent bending flexibility of tubulin regulates microtubule assembly. Nature 435(7044):911-915.
47. Franck AD, et al. (2007) Tension applied through the Dam1 complex promotes microtubule elongation providing a direct mechanism for length control in mitosis. Nat Cell Biol 9(7):832-837. (Pubitemid 47019470)
48. Rice LM, Montabana EA, Agard DA (2008) The lattice as allosteric effector: Structural studies of alphabeta- and gamma-tubulin clarify the role of GTP in microtubule assembly. Proc Natl Acad Sci USA 105(14):5378-5383. (Pubitemid 351753871)
49. Grishchuk EL, Molodtsov MI, Ataullakhanov FI, McIntosh JR (2005) Force production by disassembling microtubules. Nature 438(7066):384-388. (Pubitemid 41643957)
50. Gell C, et al. (2011) Purification of tubulin from porcine brain. Methods Mol Biol 777:15-28.
51. Gell C, et al. (2010) Microtubule dynamics reconstituted in vitro and imaged by single-molecule fluorescence microscopy. Methods Cell Biol 95:221-245.
52. Mahamdeh M, Schäffer E (2009) Optical tweezers with millikelvin precision of temperature-controlled objectives and base-pair resolution. Opt Express 17(19):17190-17199.